Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2017, Article ID 6373412, 12 pages
https://doi.org/10.1155/2017/6373412
Review Article

Circadian Plasticity of Mammalian Inhibitory Interneurons

1Department of Histology, Jagiellonian University Medical College, 7 Kopernika Street, 31-034 Krakow, Poland
2Department of Cell Biology and Imaging, Institute of Zoology, Jagiellonian University, 9 Gronostajowa Street, 30-387 Krakow, Poland

Correspondence should be addressed to Elzbieta Pyza; lp.ude.ju@azyp.ateibzle

Received 29 August 2016; Revised 15 January 2017; Accepted 19 February 2017; Published 6 March 2017

Academic Editor: Stuart C. Mangel

Copyright © 2017 Malgorzata Jasinska and Elzbieta Pyza. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. M. Reppert and D. R. Weaver, “Coordination of circadian timing in mammals,” Nature, vol. 418, no. 6901, pp. 935–941, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. J. S. Takahashi, H.-K. Hong, C. H. Ko, and E. L. McDearmon, “The genetics of mammalian circadian order and disorder: implications for physiology and disease,” Nature Reviews Genetics, vol. 9, no. 10, pp. 764–775, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Stratmann and U. Schibler, “Properties, entrainment, and physiological functions of mammalian peripheral oscillators,” Journal of Biological Rhythms, vol. 21, no. 6, pp. 494–506, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. P. L. Lowrey and J. S. Takahashi, “Genetics of circadian rhythms in mammalian model organisms,” Advances in Genetics, vol. 74, pp. 175–230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. T. S. Andreani, T. Q. Itoh, E. Yildirim, D.-S. Hwangbo, and R. Allada, “Genetics of circadian rhythms,” Sleep Medicine Clinics, vol. 10, no. 4, pp. 413–421, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Chaix, A. Zarrinpar, and S. Panda, “The circadian coordination of cell biology,” The Journal of Cell Biology, vol. 215, no. 1, pp. 15–25, 2016. View at Publisher · View at Google Scholar
  7. A. I. Gulyás, N. Hájos, I. Katona, and T. F. Freund, “Interneurons are the local targets of hippocampal inhibitory cells which project to the medial septum,” European Journal of Neuroscience, vol. 17, no. 9, pp. 1861–1872, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Caputi, S. Melzer, M. Michael, and H. Monyer, “The long and short of GABAergic neurons,” Current Opinion in Neurobiology, vol. 23, no. 2, pp. 179–186, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. E. C. Fuchs, A. Neitz, R. Pinna, S. Melzer, A. Caputi, and H. Monyer, “Local and distant input controlling excitation in layer II of the medial entorhinal cortex,” Neuron, vol. 89, no. 1, pp. 194–208, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Markram, M. Toledo-Rodriguez, Y. Wang, A. Gupta, G. Silberberg, and C. Wu, “Interneurons of the neocortical inhibitory system,” Nature Reviews Neuroscience, vol. 5, no. 10, pp. 793–807, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Klausberger and P. Somogyi, “Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations,” Science, vol. 321, no. 5885, pp. 53–57, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. X. Leinekugel, I. Khalilov, H. McLean et al., “GABA is the principal fast-acting excitatory transmitter in the neonatal brain,” Advances in Neurology, vol. 79, pp. 189–201, 1999. View at Google Scholar · View at Scopus
  13. Y. Ben-Ari, “The GABA excitatory/inhibitory developmental sequence: a personal journey,” Neuroscience, vol. 279, pp. 187–219, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Yamada, A. Okabe, H. Toyoda, W. Kilb, H. J. Luhmann, and A. Fukuda, “Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1,” Journal of Physiology, vol. 557, no. 3, pp. 829–841, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Ikeda, T. Yoshioka, and C. N. Allen, “Developmental and circadian changes in Ca2+ mobilization mediated by GABAA and NMDA receptors in the suprachiasmatic nucleus,” European Journal of Neuroscience, vol. 17, no. 1, pp. 58–70, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. R. Grantyn, C. Henneberge, R. Jüttner, J. C. Meier, and S. Kirischuk, “Functional hallmarks of GABAergic synapse maturation and the diverse roles of neurotrophins,” Frontiers in Cellular Neuroscience, vol. 5, article no. 13, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. I. Khalilov, M. Minlebaev, M. Mukhtarov, and R. Khazipov, “Dynamic changes from depolarizing to hyperpolarizing GABAergic actions during giant depolarizing potentials in the neonatal rat hippocampus,” Journal of Neuroscience, vol. 35, no. 37, pp. 12635–12642, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Fujiwara-Tsukamoto, Y. Isomura, M. Imanishi, T. Fukai, and M. Takada, “Distinct types of ionic modulation of GABA actions in pyramidal cells and interneurons during electrical induction of hippocampal seizure-like network activity,” European Journal of Neuroscience, vol. 25, no. 9, pp. 2713–2725, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Viitanen, E. Ruusuvuori, K. Kaila, and J. Voipio, “The K+-Cl- cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus,” Journal of Physiology, vol. 588, no. 9, pp. 1527–1540, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Wagner, M. Castel, H. Gainer, and Y. Yarom, “GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity,” Nature, vol. 387, no. 6633, pp. 598–603, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. M. De Jeu and C. Pennartz, “Circadian modulation of GABA function in the rat suprachiasmatic nucleus: excitatory effects during the night phase,” Journal of Neurophysiology, vol. 87, no. 2, pp. 834–844, 2002. View at Google Scholar · View at Scopus
  22. L. M. Grover, N. A. Lambert, P. A. Schwartzkroin, and T. J. Teyler, “Role of HCO3- ions in depolarizing GABA(A) receptor-mediated responses in pyramidal cells of rat hippocampus,” Journal of Neurophysiology, vol. 69, no. 5, pp. 1541–1555, 1993. View at Google Scholar · View at Scopus
  23. T. F. Freund and G. Buzsáki, “Interneurons of the Hippocampus,” Hippocampus, vol. 6, no. 4, pp. 347–470, 1996. View at Google Scholar · View at Scopus
  24. K. Kaila, K. Lamsa, S. Smirnov, T. Taira, and J. Voipio, “Long-lasting GABA-mediated depolarization evoked by high-frequency stimulation in pyramidal neurons of rat hippocampal slice is attributable to a network-driven, bicarbonate-dependent K+ transient,” Journal of Neuroscience, vol. 17, no. 20, pp. 7662–7672, 1997. View at Google Scholar · View at Scopus
  25. J. C. Hee, C. J. Lee, A. Schroeder et al., “Excitatory actions of GABA in the suprachiasmatic nucleus,” Journal of Neuroscience, vol. 28, no. 21, pp. 5450–5459, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. R. P. Irwin and C. N. Allen, “GABAergic signaling induces divergent neuronal Ca2+ responses in the suprachiasmatic nucleus network,” European Journal of Neuroscience, vol. 30, no. 8, pp. 1462–1475, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Alamilla, A. Perez-Burgos, D. Quinto, and R. Aguilar-Roblero, “Circadian modulation of the Cl- equilibrium potential in the rat suprachiasmatic nuclei,” BioMed Research International, vol. 2014, Article ID 424982, 15 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. V. K. Gribkoff, R. L. Pieschl, and F. E. Dudek, “GABA receptor-mediated inhibition of neuronal activity in rat SCN in vitro: pharmacology and influence of circadian phase,” Journal of Neurophysiology, vol. 90, no. 3, pp. 1438–1448, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Albus, M. J. Vansteensel, S. Michel, G. D. Block, and J. H. Meijer, “A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock,” Current Biology, vol. 15, no. 10, pp. 886–893, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Belenky, Y. Yarom, and G. E. Pickard, “Heterogeneous expression of γ-aminobutyric acid and γ-aminobutyric acid-associated receptors and transporters in the rat suprachiasmatic nucleus,” Journal of Comparative Neurology, vol. 506, no. 4, pp. 708–732, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. E. O. Mann and O. Paulsen, “Role of GABAergic inhibition in hippocampal network oscillations,” Trends in Neurosciences, vol. 30, no. 7, pp. 343–349, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. J. S. Isaacson and M. Scanziani, “How inhibition shapes cortical activity,” Neuron, vol. 72, no. 2, pp. 231–243, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Bannai, F. Niwa, M. W. Sherwood et al., “Bidirectional control of synaptic GABAAR clustering by glutamate and calcium,” Cell Reports, vol. 13, no. 12, pp. 2768–2780, 2015. View at Publisher · View at Google Scholar · View at Scopus
  34. S. R. Cobb, E. H. Buhl, K. Halasy, O. Paulsen, and P. Somogyi, “Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons,” Nature, vol. 378, no. 6552, pp. 75–78, 1995. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Liu and S. M. Reppert, “GABA synchronizes clock cells within the suprachiasmatic circadian clock,” Neuron, vol. 25, no. 1, pp. 123–128, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Klausberger, P. J. Magill, L. F. Márton et al., “Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo,” Nature, vol. 421, no. 6925, pp. 844–848, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. E. Stark, R. Eichler, L. Roux, S. Fujisawa, H. G. Rotstein, and G. Buzsáki, “Inhibition-induced theta resonance in cortical circuits,” Neuron, vol. 80, no. 5, pp. 1263–1276, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. J. A. Evans, T. L. Leise, O. Castanon-Cervantes, and A. J. Davidson, “Dynamic interactions mediated by nonredundant signaling mechanisms couple circadian clock neurons,” Neuron, vol. 80, no. 4, pp. 973–983, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. G. M. Freeman, R. M. Krock, S. J. Aton, P. Thaben, and E. D. Herzog, “GABA networks destabilize genetic oscillations in the circadian pacemaker,” Neuron, vol. 78, no. 5, pp. 799–806, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. D. DeWoskin, J. Myung, M. D. C. Belle, H. D. Piggins, T. Takumi, and D. B. Forger, “Distinct roles for GABA across multiple timescales in mammalian circadian timekeeping,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 29, pp. E3911–E3919, 2015. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Farajnia, T. Deboer, J. H. T. Rohling, J. H. Meijer, and S. Michel, “Aging of the suprachiasmatic clock,” Neuroscientist, vol. 20, no. 1, pp. 44–55, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. J. F. Duffy, K.-M. Zitting, and E. D. Chinoy, “Aging and circadian rhythms,” Sleep Medicine Clinics, vol. 10, no. 4, pp. 423–434, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Banks, P. M. Nolan, and S. N. Peirson, “Reciprocal interactions between circadian clocks and aging,” Mammalian Genome, vol. 27, no. 7-8, pp. 332–340, 2016. View at Publisher · View at Google Scholar · View at Scopus
  44. M. J. Duncan, J. M. Herron, and S. A. Hill, “Aging selectively suppresses vasoactive intestinal peptide messenger RNA expression in the suprachiasmatic nucleus of the Syrian hamster,” Molecular Brain Research, vol. 87, no. 2, pp. 196–203, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Palomba, M. Nygård, F. Florenzano, G. Bertini, K. Kristensson, and M. Bentivoglio, “Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse,” Journal of Biological Rhythms, vol. 23, no. 3, pp. 220–231, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Nygård and M. Palomba, “The GABAergic network in the suprachiasmatic nucleus as a key regulator of the biological clock: does it change during senescence?” Chronobiology International, vol. 23, no. 1-2, pp. 427–435, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. S. L. Chellappa, G. Gaggioni, J. Q. Ly et al., “Circadian dynamics in measures of cortical excitation and inhibition balance,” Scientific Reports, vol. 6, article 33661, 2016. View at Publisher · View at Google Scholar
  48. A. Satlin, L. Volicer, E. G. Stopa, and D. Harper, “Circadian locomotor activity and core-body temperature rhythms in Alzheimer's disease,” Neurobiology of Aging, vol. 16, no. 5, pp. 765–771, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. Y.-H. Wu and D. F. Swaab, “Disturbance and strategies for reactivation of the circadian rhythm system in aging and Alzheimer's disease,” Sleep Medicine, vol. 8, no. 6, pp. 623–636, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Videnovic and G. L. Willis, “Circadian system—a novel diagnostic and therapeutic target in Parkinson's disease?” Movement Disorders, vol. 31, no. 3, pp. 260–269, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. D. B. Boivin, “Influence of sleep-wake and circadian rhythm disturbances in psychiatric disorders,” Journal of Psychiatry and Neuroscience, vol. 25, no. 5, pp. 446–458, 2000. View at Google Scholar · View at Scopus
  52. K. Wulff, D.-J. Dijk, B. Middleton, R. G. Foster, and E. M. Joyce, “Sleep and circadian rhythm disruption in schizophrenia,” British Journal of Psychiatry, vol. 200, no. 4, pp. 308–316, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Jacob, “Cortical interneuron dysfunction in epilepsy associated with autism spectrum disorders,” Epilepsia, vol. 57, no. 2, pp. 182–193, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Roenneberg, K. V. Allebrandt, M. Merrow, and C. Vetter, “Social jetlag and obesity,” Current Biology, vol. 22, no. 10, pp. 939–943, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. F. A. J. L. Scheer, M. F. Hilton, C. S. Mantzoros, and S. A. Shea, “Adverse metabolic and cardiovascular consequences of circadian misalignment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 11, pp. 4453–4458, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Y. Moore and J. C. Speh, “GABA is the principal neurotransmitter of the circadian system,” Neuroscience Letters, vol. 150, no. 1, pp. 112–116, 1993. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Bouskila and F. E. Dudek, “Neuronal synchronization without calcium-dependent synaptic transmission in the hypothalamus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 8, pp. 3207–3210, 1993. View at Publisher · View at Google Scholar · View at Scopus
  58. D. K. Welsh, D. E. Logothetis, M. Meister, and S. M. Reppert, “Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms,” Neuron, vol. 14, no. 4, pp. 697–706, 1995. View at Publisher · View at Google Scholar · View at Scopus
  59. A.-M. François-Bellan, L. Segu, and M. Héry, “Regulation by estradiol of GABAA and GABAB binding sites in the diencephalon of the rat: an autoradiographic study,” Brain Research, vol. 503, no. 1, pp. 144–147, 1989. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Y. Liou and H. E. Albers, “Single unit response of neurons within the hamster suprachiasmatic nucleus to GABA and low chloride perfusate during the day and night,” Brain Research Bulletin, vol. 25, no. 1, pp. 93–98, 1990. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Y. Moore, J. C. Speh, and R. K. Leak, “Suprachiasmatic nucleus organization,” Cell and Tissue Research, vol. 309, no. 1, pp. 89–98, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. L. P. Morin and C. N. Allen, “The circadian visual system, 2005,” Brain Research Reviews, vol. 51, no. 1, pp. 1–60, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. J. D. Mikkelsen and J. Fahrenkrug, “Concentrations and distribution of vasoactive intestinal peptide (VIP), peptide histidine isoleucine (PHI) and peptide histidine valine (PHV) in the cerebral cortex and the suprachiasmatic nucleus of the mouse,” Brain Research, vol. 656, no. 1, pp. 95–107, 1994. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Y. Moore, “Entrainment pathways and the functional organization of the circadian system,” Progress in Brain Research, vol. 111, pp. 103–119, 1996. View at Publisher · View at Google Scholar · View at Scopus
  65. E. E. Abrahamson and R. Y. Moore, “Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections,” Brain Research, vol. 916, no. 1-2, pp. 172–191, 2001. View at Publisher · View at Google Scholar · View at Scopus
  66. L. P. Morin, K.-Y. Shivers, J. H. Blanchard, and L. Muscat, “Complex organization of mouse and rat suprachiasmatic nucleus,” Neuroscience, vol. 137, no. 4, pp. 1285–1297, 2006. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Schaap, C. M. A. Pennartz, and J. H. Meijer, “Electrophysiology of the circadian pacemaker in mammals,” Chronobiology International, vol. 20, no. 2, pp. 171–188, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. C. S. Colwell, “Linking neural activity and molecular oscillations in the SCN,” Nature Reviews Neuroscience, vol. 12, no. 10, pp. 553–569, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. J. R. Jones and D. G. McMahon, “The core clock gene Per1 phases molecular and electrical circadian rhythms in SCN neurons,” PeerJ, vol. 4, p. e2297, 2016. View at Publisher · View at Google Scholar
  70. Z.-G. Jiang, Y. Yang, Z.-P. Liu, and C. N. Allen, “Membrane properties and synaptic inputs of suprachiasmatic nucleus neurons in rat brain slices,” Journal of Physiology, vol. 499, no. 1, pp. 141–159, 1997. View at Publisher · View at Google Scholar · View at Scopus
  71. H. S. Gompf and C. N. Allen, “GABAergic synapses of the suprachiasmatic nucleus exhibit a diurnal rhythm of short-term synaptic plasticity,” European Journal of Neuroscience, vol. 19, no. 10, pp. 2791–2798, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. S. J. Aton, J. E. Huettner, M. Straume, and E. D. Herzog, “GABA and Gi/o differentially control circadian rhythms and synchrony in clock neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 50, pp. 19188–19193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Vasalou, E. D. Herzog, and M. A. Henson, “Multicellular model for intercellular synchronization in circadian neural networks,” Biophysical Journal, vol. 101, no. 1, pp. 12–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Hamada and S. Shibata, “The role of GABAergic neuron on NMDA- and SP-induced phase delays in the suprachiasmatic nucleus neuronal activity rhythm in vitro,” Neuroscience Letters, vol. 468, no. 3, pp. 344–347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. D. L. Hummer, J. C. Ehlen, T. E. Larkin et al., “Sustained activation of GABAA receptors in the suprachiasmatic nucleus mediates light-induced phase delays of the circadian clock: a novel function of ionotropic receptors,” European Journal of Neuroscience, vol. 42, no. 2, pp. 1830–1838, 2015. View at Publisher · View at Google Scholar · View at Scopus
  76. N. J. Kingsbury, S. R. Taylor, and M. A. Henson, “Inhibitory and excitatory networks balance cell coupling in the suprachiasmatic nucleus: a modeling approach,” Journal of Theoretical Biology, vol. 397, pp. 135–144, 2016. View at Publisher · View at Google Scholar
  77. H. E. Albers, J. C. Walton, K. L. Gamble, J. K. McNeill, and D. L. Hummer, “The dynamics of GABA signaling: revelations from the circadian pacemaker in the suprachiasmatic nucleus,” Frontiers in Neuroendocrinology, vol. 44, pp. 35–82, 2017. View at Publisher · View at Google Scholar
  78. J. Itri and C. S. Colwell, “Regulation of inhibitory synaptic transmission by vasoactive intestinal peptide (VIP) in the mouse suprachiasmatic nucleus,” Journal of Neurophysiology, vol. 90, no. 3, pp. 1589–1597, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. J. Itri, S. Michel, J. A. Waschek, and C. S. Colwell, “Circadian rhythm in inhibitory synaptic transmission in the mouse suprachiasmatic nucleus,” Journal of Neurophysiology, vol. 92, no. 1, pp. 311–319, 2004. View at Publisher · View at Google Scholar · View at Scopus
  80. R. Aguilar-Roblero, L. Verduzco-Carbajal, C. Rodríguez, J. Mendez-Franco, J. Morán, and M. P. de la Mora, “Circadian rhythmicity in the GABAergic system in the suprachiasmatic nuclei of the rat,” Neuroscience Letters, vol. 157, no. 2, pp. 199–202, 1993. View at Publisher · View at Google Scholar · View at Scopus
  81. K. L. Huhman, A. C. Hennessey, and H. E. Albers, “Rhythms of glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus,” Journal of Biological Rhythms, vol. 11, no. 4, pp. 311–316, 1996. View at Publisher · View at Google Scholar · View at Scopus
  82. K. L. Huhman, A. M. Jasnow, A. K. Sisitsky, and H. E. Albers, “Glutamic acid decarboxylase mRNA in the suprachiasmatic nucleus of rats housed in constant darkness,” Brain Research, vol. 851, no. 1-2, pp. 266–269, 1999. View at Publisher · View at Google Scholar · View at Scopus
  83. K. Shinohara, T. Funabashi, and F. Kimura, “Temporal profiles of vasoactive intestinal polypeptide precursor mRNA and its receptor mRNA in the rat suprachiasmatic nucleus,” Molecular Brain Research, vol. 63, no. 2, pp. 262–267, 1999. View at Publisher · View at Google Scholar · View at Scopus
  84. H. E. Albers, E. G. Stopa, R. T. Zoeller et al., “Day-night variation in prepro vasoactive intestinal peptide/peptide histidine isoleucine mRNA within the rat suprachiasmatic nucleus,” Molecular Brain Research, vol. 7, no. 1, pp. 85–89, 1990. View at Publisher · View at Google Scholar · View at Scopus
  85. H. E. Albers, N. Minamitani, E. Stopa, and C. F. Ferris, “Light selectively alters vasoactive intestinal peptide and peptide histidine isoleucine immunoreactivity within the rat suprachiasmatic nucleus,” Brain Research, vol. 437, no. 1, pp. 189–192, 1987. View at Publisher · View at Google Scholar · View at Scopus
  86. J. M. Francl, G. Kaur, and J. D. Glass, “Regulation of vasoactive intestinal polypeptide release in the suprachiasmatic nucleus circadian clock,” NeuroReport, vol. 21, no. 16, pp. 1055–1059, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Lesauter, T. Bhuiyan, T. Shimazoe, and R. Silver, “Circadian trafficking of calbindin-ir in fibers of SCN neurons,” Journal of Biological Rhythms, vol. 24, no. 6, pp. 488–496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. F. H. Güldner and C. A. Ingham, “Plasticity in synaptic appositions of optic nerve afferents under different lighting conditions,” Neuroscience Letters, vol. 14, no. 2-3, pp. 235–240, 1979. View at Publisher · View at Google Scholar · View at Scopus
  89. D. Becquet, C. Girardet, F. Guillaumond, A.-M. François-Bellan, and O. Bosler, “Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment,” GLIA, vol. 56, no. 3, pp. 294–305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. C. Girardet, M.-P. Blanchard, G. Ferracci et al., “Daily changes in synaptic innervation of VIP neurons in the rat suprachiasmatic nucleus: contribution of glutamatergic afferents,” European Journal of Neuroscience, vol. 31, no. 2, pp. 359–370, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. J. L. Mosinger, S. Yazulla, and K. M. Studholme, “GABA-like immunoreactivity in the vertebrate retina: a species comparison,” Experimental Eye Research, vol. 42, no. 6, pp. 631–644, 1986. View at Publisher · View at Google Scholar · View at Scopus
  92. N. Vardi, D. L. Kaufman, and P. Sterling, “Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase,” Visual Neuroscience, vol. 11, no. 1, pp. 135–142, 1994. View at Publisher · View at Google Scholar · View at Scopus
  93. N. Menger, D. V. Pow, and H. Wässle, “Glycinergic amacrine cells of the rat retina,” Journal of Comparative Neurology, vol. 401, no. 1, pp. 34–46, 1998. View at Publisher · View at Google Scholar · View at Scopus
  94. J. Crooks and H. Kolb, “Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina,” Journal of Comparative Neurology, vol. 315, no. 3, pp. 287–302, 1992. View at Publisher · View at Google Scholar · View at Scopus
  95. A. E. Chávez, W. N. Grimes, and J. S. Diamond, “Mechanisms underlying lateral GABAergic feedback onto rod bipolar cells in rat retina,” Journal of Neuroscience, vol. 30, no. 6, pp. 2330–2339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. D. I. Vaney and H. M. Young, “GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina,” Brain Research, vol. 438, no. 1-2, pp. 369–373, 1988. View at Publisher · View at Google Scholar · View at Scopus
  97. H. Hirasawa, R. A. Betensky, and E. Raviola, “Corelease of dopamine and GABA by a retinal dopaminergic neuron,” Journal of Neuroscience, vol. 32, no. 38, pp. 13281–13291, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. R. G. Pourcho and D. J. Goebel, “Colocalization of substance P and γ-aminobutyric acid in amacrine cells of the cat retina,” Brain Research, vol. 447, no. 1, pp. 164–168, 1988. View at Publisher · View at Google Scholar · View at Scopus
  99. D. W. Marshak, “Peptidergic neurons of the macaque monkey retina,” Neuroscience Research Supplements, vol. 10, pp. S117–S130, 1989. View at Publisher · View at Google Scholar · View at Scopus
  100. H. Wässle, U. Grünert, and J. Röhrenbeck, “Immunocytochemical staining of AII-amacrine cells in the rat retina with antibodies against parvalbumin,” Journal of Comparative Neurology, vol. 332, no. 4, pp. 407–420, 1993. View at Publisher · View at Google Scholar · View at Scopus
  101. D. J. Goebel and R. G. Pourcho, “Calretinin in the cat retina: colocalizations with other calcium-binding proteins, GABA and glycine,” Visual Neuroscience, vol. 14, no. 2, pp. 311–322, 1997. View at Publisher · View at Google Scholar · View at Scopus
  102. C. O. Jaliffa, D. Saenz, E. Resnik, M. I. Keller Sarmiento, and R. E. Rosenstein, “Circadian activity of the GABAergic system in the golden hamster retina,” Brain Research, vol. 912, no. 2, pp. 195–202, 2001. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Gábriel, J. Lesauter, T. Bánvölgyi, G. Petrovics, R. Silver, and P. Witkovsky, “AII amacrine neurons of the rat retina show diurnal and circadian rhythms of parvalbumin immunoreactivity,” Cell and Tissue Research, vol. 315, no. 2, pp. 181–186, 2004. View at Publisher · View at Google Scholar · View at Scopus
  104. R. Gabriel, J. Lesauter, R. Silver, A. Garcia-Espaa, and P. Witkovsky, “Diurnal and circadian variation of protein kinase C immunoreactivity in the rat retina,” Journal of Comparative Neurology, vol. 439, no. 2, pp. 140–150, 2001. View at Publisher · View at Google Scholar · View at Scopus
  105. E. L. White, Cortical Circuits: Synaptic Organization of the Cerebral Cortex: Structure, Function and theory, edited by E. L. White and A. Keller, Birkhäuser, Boston, Mass, USA, 1989.
  106. A. M. Thomson and J. Deuchars, “Temporal and spatial properties of local circuits in neocortex,” Trends in Neurosciences, vol. 17, no. 3, pp. 119–126, 1994. View at Publisher · View at Google Scholar · View at Scopus
  107. K. Letinic, R. Zoncu, and P. Rakic, “Origin of GABAergic neurons in the human neocortex,” Nature, vol. 417, no. 6889, pp. 645–649, 2002. View at Publisher · View at Google Scholar · View at Scopus
  108. J. DeFelipe, “Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex,” Journal of Chemical Neuroanatomy, vol. 14, no. 1, pp. 1–19, 1997. View at Publisher · View at Google Scholar · View at Scopus
  109. B. I. Kanterewicz, D. A. Golombek, R. E. Rosenstein, and D. P. Cardinali, “Diurnal changes of GABA turnover rate in brain and pineal gland of Syrian hamsters,” Brain Research Bulletin, vol. 31, no. 6, pp. 661–666, 1993. View at Publisher · View at Google Scholar · View at Scopus
  110. B. I. Kanterewicz, R. E. Rosenstein, D. A. Golombek, P. C. Yannielli, and D. P. Cardinali, “Daily variations in GABA receptor function in Syrian hamster cerebral cortex,” Neuroscience Letters, vol. 200, no. 3, pp. 211–213, 1995. View at Publisher · View at Google Scholar · View at Scopus
  111. C. J. Evans, D. J. McGonigle, and R. A. E. Edden, “Diurnal stability of γ-aminobutyric acid concentration in visual and sensorimotor cortex,” Journal of Magnetic Resonance Imaging, vol. 31, no. 1, pp. 204–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. S. H. Doeltgen and M. C. Ridding, “Behavioural exposure and sleep do not modify corticospinal and intracortical excitability in the human motor system,” Clinical Neurophysiology, vol. 121, no. 3, pp. 448–452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  113. M. Jasińska, A. Grzegorczyk, E. Jasek et al., “Daily rhythm of synapse turnover in mouse somatosensory cortex,” Acta Neurobiologiae Experimentalis, vol. 74, no. 1, pp. 104–110, 2014. View at Google Scholar · View at Scopus
  114. M. Jasinska, A. Grzegorczyk, O. Woznicka et al., “Circadian rhythmicity of synapses in mouse somatosensory cortex,” European Journal of Neuroscience, vol. 42, no. 8, pp. 2585–2594, 2015. View at Publisher · View at Google Scholar · View at Scopus
  115. K. Fox, “Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex,” Neuroscience, vol. 111, no. 4, pp. 799–814, 2002. View at Publisher · View at Google Scholar · View at Scopus
  116. G. Tamás, E. H. Buhl, and P. Somogyi, “Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex,” Journal of Physiology, vol. 500, no. 3, pp. 715–738, 1997. View at Publisher · View at Google Scholar · View at Scopus
  117. P. Somogyi, T. F. Freund, A. J. Hodgson, J. Somogyi, D. Beroukas, and I. W. Chubb, “Identified axo-axonic cells are immunoreactive for GABA in the hippocampus visual cortex of the cat,” Brain Research, vol. 332, no. 1, pp. 143–149, 1985. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Halasy, S. R. Cobb, E. H. Buhl, G. Nyiri, and P. Somogyi, “Sites of synaptic junctions established by a GABAergic basket cell on an interneuron in the CA1 area of the rat hippocampus,” Neurobiology, vol. 4, no. 3, pp. 269–270, 1996. View at Google Scholar · View at Scopus
  119. T. Klausberger, “GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus,” European Journal of Neuroscience, vol. 30, no. 6, pp. 947–957, 2009. View at Publisher · View at Google Scholar · View at Scopus
  120. L. Acsády, D. Arabadzisz, and T. F. Freund, “Correlated morphological and neurochemical features identify different subsets of vasoactive intestinal polypeptide-immunoreactive interneurons in rat hippocampus,” Neuroscience, vol. 73, no. 2, pp. 299–315, 1996. View at Publisher · View at Google Scholar · View at Scopus
  121. C. J. McBain, T. F. Freund, and I. Mody, “Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity,” Trends in Neurosciences, vol. 22, no. 5, pp. 228–235, 1999. View at Publisher · View at Google Scholar · View at Scopus
  122. K. M. Harris and T. J. Teyler, “Age differences in a circadian influence on hippocamapl LTP,” Brain Research, vol. 261, no. 1, pp. 69–73, 1983. View at Publisher · View at Google Scholar · View at Scopus
  123. A. V. Raghavan, J. M. Horowitz, and C. A. Fuller, “Diurnal modulation of long-term potentiation in the hamster hippocampal slice,” Brain Research, vol. 833, no. 2, pp. 311–314, 1999. View at Publisher · View at Google Scholar · View at Scopus
  124. H. Nakatsuka and K. Natsume, “Circadian rhythm modulates long-term potentiation induced at CA1 in rat hippocampal slices,” Neuroscience Research, vol. 80, no. 1, pp. 1–9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. D. Chaudhury, L. M. Wang, and C. S. Colwell, “Circadian regulation of hippocampal long-term potentiation,” Journal of Biological Rhythms, vol. 20, no. 3, pp. 225–236, 2005. View at Publisher · View at Google Scholar · View at Scopus
  126. V. Egger, K. Svoboda, and Z. F. Mainen, “Dendrodendritic synaptic signals in olfactory bulb granule cells: local spine boost and global low-threshold spike,” Journal of Neuroscience, vol. 25, no. 14, pp. 3521–3530, 2005. View at Publisher · View at Google Scholar · View at Scopus
  127. H.-W. Dong, A. Hayar, and M. Ennis, “Activation of group I metabotropic glutamate receptors on main olfactory bulb granule cells and periglomerular cells enhances synaptic inhibition of mitral cells,” Journal of Neuroscience, vol. 27, no. 21, pp. 5654–5663, 2007. View at Publisher · View at Google Scholar · View at Scopus
  128. J. S. Isaacson, “Mechanisms governing dendritic γ-aminobutyric acid (GABA) release in the rat olfactory bulb,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 1, pp. 337–342, 2001. View at Publisher · View at Google Scholar · View at Scopus
  129. D. Arruda, R. Publio, and A. C. Roque, “The periglomerular cell of the olfactory bulb and its role in controlling mitral cell spiking: a computational model,” PLoS ONE, vol. 8, no. 2, Article ID e56148, 2013. View at Publisher · View at Google Scholar · View at Scopus
  130. B. J. Maher and G. L. Westbrook, “Co-transmission of dopamine and GABA in periglomerular cells,” Journal of Neurophysiology, vol. 99, no. 3, pp. 1559–1564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. J.-E. K. Miller, D. Granados-Fuentes, T. Wang, L. Marpegan, T. E. Holy, and E. D. Herzog, “Vasoactive intestinal polypeptide mediates circadian rhythms in mammalian olfactory bulb and olfaction,” Journal of Neuroscience, vol. 34, no. 17, pp. 6040–6046, 2014. View at Publisher · View at Google Scholar · View at Scopus
  132. D. Granados-Fuentes, M. T. Saxena, L. M. Prolo, S. J. Aton, and E. D. Herzog, “Olfactory bulb neurons express functional, entrainable circadian rhythms,” European Journal of Neuroscience, vol. 19, no. 4, pp. 898–906, 2004. View at Publisher · View at Google Scholar · View at Scopus
  133. D. Granados-Fuentes, G. Ben-Josef, G. Perry, D. A. Wilson, A. Sullivan-Wilson, and E. D. Herzog, “Daily rhythms in olfactory discrimination depend on clock genes but not the suprachiasmatic nucleus,” Journal of Biological Rhythms, vol. 26, no. 6, pp. 552–560, 2011. View at Publisher · View at Google Scholar · View at Scopus
  134. U. Abraham, J. L. Prior, D. Granados-Fuentes, D. R. Piwnica-Worms, and E. D. Herzog, “Independent circadian oscillations of Period1 in specific brain areas in vivo and in vitro,” Journal of Neuroscience, vol. 25, no. 38, pp. 8620–8626, 2005. View at Publisher · View at Google Scholar · View at Scopus
  135. D. Granados-Fuentes, L. M. Prolo, U. Abraham, and E. D. Herzog, “The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb,” Journal of Neuroscience, vol. 24, no. 3, pp. 615–619, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. E. De Schutter, B. Vos, and R. Maex, “The function of cerebellar Golgi cells revisited,” Progress in Brain Research, vol. 124, pp. 81–93, 2000. View at Google Scholar · View at Scopus
  137. H. Korn and H. Axelrad, “Electrical inhibition of Purkinje cells in the cerebellum of the rat,” Proceedings of the National Academy of Sciences of the United States of America, vol. 77, no. 10, pp. 6244–6247, 1980. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Lainé and H. Axelrad, “Lugaro cells target basket and stellate cells in the cerebellar cortex,” NeuroReport, vol. 9, no. 10, pp. 2399–2403, 1998. View at Publisher · View at Google Scholar · View at Scopus
  139. M. Fortin, R. Marchand, and A. Parent, “Calcium-binding proteins in primate cerebellum,” Neuroscience Research, vol. 30, no. 2, pp. 155–168, 1998. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Rickmann and J. R. Wolff, “S100 protein expression in subpopulations of neurons of rat brain,” Neuroscience, vol. 67, no. 4, pp. 977–991, 1995. View at Publisher · View at Google Scholar · View at Scopus
  141. J. Mendoza, P. Pévet, M.-P. Felder-Schmittbuhl, Y. Bailly, and E. Challet, “The cerebellum harbors a circadian oscillator involved in food anticipation,” Journal of Neuroscience, vol. 30, no. 5, pp. 1894–1904, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. M. F. Rath, L. Rovsing, and M. Møller, “Circadian oscillators in the mouse brain: molecular clock components in the neocortex and cerebellar cortex,” Cell and Tissue Research, vol. 357, no. 3, pp. 743–755, 2014. View at Publisher · View at Google Scholar · View at Scopus
  143. Y. Kawaguchi, C. J. Wilson, S. J. Augood, and P. C. Emson, “Striatal interneurones: chemical, physiological and morphological characterization,” Trends in Neurosciences, vol. 18, no. 12, pp. 527–535, 1995. View at Publisher · View at Google Scholar · View at Scopus
  144. J. M. Tepper, F. Tecuapetla, T. Koós, and O. Ibáñez-Sandoval, “Heterogeneity and diversity of striatal GABAergic interneurons,” Frontiers in Neuroanatomy, 2010. View at Publisher · View at Google Scholar · View at Scopus
  145. J. P. Bolam, D. J. Clarke, A. D. Smith, and P. Somogyi, “A type of aspiny neuron in the rat neostriatum accumulates [3H]γ-aminobutyric acid: combination of Golgi-staining, autoradiography, and electron microscopy,” Journal of Comparative Neurology, vol. 213, no. 2, pp. 121–134, 1983. View at Publisher · View at Google Scholar · View at Scopus
  146. Y. Kawaguchi, “Neostriatal cell subtypes and their functional roles,” Neuroscience Research, vol. 27, no. 1, pp. 1–8, 1997. View at Publisher · View at Google Scholar · View at Scopus
  147. S. R. Lapper and J. P. Bolam, “Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat,” Neuroscience, vol. 51, no. 3, pp. 533–545, 1992. View at Publisher · View at Google Scholar · View at Scopus
  148. B. D. Bennett and J. P. Bolam, “Characterization of calretinin-immunoreactive structures in the striatum of the rat,” Brain Research, vol. 609, no. 1-2, pp. 137–148, 1993. View at Publisher · View at Google Scholar · View at Scopus
  149. M. Cossette, D. Lévesque, and A. Parent, “Neurochemical characterization of dopaminergic neurons in human striatum,” Parkinsonism and Related Disorders, vol. 11, no. 5, pp. 277–286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  150. T. R. Castañeda, B. Marquez De Prado, D. Prieto, and F. Mora, “Circadian rhythms of dopamine, glutamate and GABA in the striatum and nucleus accumbens of the awake rat: modulation by light,” Journal of Pineal Research, vol. 36, no. 3, pp. 177–185, 2004. View at Publisher · View at Google Scholar · View at Scopus
  151. M. Verwey, S. Dhir, and S. Amir, “Circadian influences on dopamine circuits of the brain: regulation of striatal rhythms of clock gene expression and implications for psychopathology and disease,” F1000Research, vol. 5, 2016. View at Publisher · View at Google Scholar
  152. C. A. McClung, “Circadian genes, rhythms and the biology of mood disorders,” Pharmacology and Therapeutics, vol. 114, no. 2, pp. 222–232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  153. E. Falcon, A. Ozburn, S. Mukherjee, K. Roybal, and C. A. McClung, “Differential regulation of the period genes in striatal regions following cocaine exposure,” PLoS ONE, vol. 8, no. 6, Article ID e66438, 2013. View at Publisher · View at Google Scholar · View at Scopus
  154. H. Braak, E. Ghebremedhin, U. Rüb, H. Bratzke, and K. Del Tredici, “Stages in the development of Parkinson's disease-related pathology,” Cell and Tissue Research, vol. 318, no. 1, pp. 121–134, 2004. View at Publisher · View at Google Scholar · View at Scopus
  155. J. W. Błaszczyk, “Parkinson's disease and neurodegeneration: GABA-collapse hypothesis,” Frontiers in Neuroscience, vol. 10, article no. 269, 2016. View at Publisher · View at Google Scholar · View at Scopus
  156. B. T. Hawkins and T. P. Davis, “The blood-brain barrier/neurovascular unit in health and disease,” Pharmacological Reviews, vol. 57, no. 2, pp. 173–185, 2005. View at Publisher · View at Google Scholar · View at Scopus
  157. D. L. Whitehead, A. D. M. Davies, J. R. Playfer, and C. J. Turnbull, “Circadian rest-activity rhythm is altered in Parkinson's disease patients with hallucinations,” Movement Disorders, vol. 23, no. 8, pp. 1137–1145, 2008. View at Publisher · View at Google Scholar · View at Scopus
  158. D. Devos, M. Kroumova, R. Bordet et al., “Heart rate variability and parkinson's disease severity,” Journal of Neural Transmission, vol. 110, no. 9, pp. 997–1011, 2003. View at Publisher · View at Google Scholar · View at Scopus
  159. A. A. Ejaz, I. S. Sekhon, and S. Munjal, “Characteristic findings on 24-h ambulatory blood pressure monitoring in a series of patients with Parkinson's disease,” European Journal of Internal Medicine, vol. 17, no. 6, pp. 417–420, 2006. View at Publisher · View at Google Scholar · View at Scopus
  160. A. Hayashi, N. Matsunaga, H. Okazaki et al., “A disruption mechanism of the molecular clock in a MPTP mouse model of Parkinson's disease,” NeuroMolecular Medicine, vol. 15, no. 2, pp. 238–251, 2013. View at Publisher · View at Google Scholar · View at Scopus
  161. R. Ito, T. W. Robbins, and B. J. Everitt, “Differential control over cocaine-seeking behavior by nucleus accumbens core and shell,” Nature Neuroscience, vol. 7, no. 4, pp. 389–397, 2004. View at Publisher · View at Google Scholar · View at Scopus
  162. L. H. Corbit, S. C. Fischbach, and P. H. Janak, “Nucleus accumbens core and shell are differentially involved in general and outcome-specific forms of Pavlovian-instrumental transfer with alcohol and sucrose rewards,” European Journal of Neuroscience, vol. 43, no. 9, pp. 1229–1236, 2016. View at Publisher · View at Google Scholar · View at Scopus
  163. C. S. Tanaka, K. Doya, G. Okada, K. Ueda, Y. Okamoto, and S. Yamawaki, “Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops,” Nature Neuroscience, vol. 7, no. 8, pp. 887–893, 2004. View at Publisher · View at Google Scholar · View at Scopus
  164. W. Schultz, “Behavioral theories and the neurophysiology of reward,” Annual Review of Psychology, vol. 57, pp. 87–115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  165. F. C. Cruz, K. R. Babin, R. M. Leao et al., “Role of nucleus accumbens shell neuronal ensembles in context-induced reinstatement of cocaine-seeking,” Journal of Neuroscience, vol. 34, no. 22, pp. 7437–7446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  166. C. J. Perry and G. P. McNally, “μ-Opioid receptors in the nucleus accumbens shell mediate context-induced reinstatement (renewal) but not primed reinstatement of extinguished alcohol seeking,” Behavioral Neuroscience, vol. 127, no. 4, pp. 535–543, 2013. View at Publisher · View at Google Scholar · View at Scopus
  167. F. J. Rubio, Q.-R. Liu, X. Li et al., “Context-induced reinstatement of methamphetamine seeking is associated with unique molecular alterations in fos-expressing dorsolateral striatum neurons,” Journal of Neuroscience, vol. 35, no. 14, pp. 5625–5639, 2015. View at Publisher · View at Google Scholar · View at Scopus
  168. D.-L. Jiao, Y. Liu, J.-D. Long et al., “Involvement of dorsal striatal α1-containing GABAA receptors in methamphetamine-associated rewarding memories,” Neuroscience, vol. 320, pp. 230–238, 2016. View at Publisher · View at Google Scholar · View at Scopus
  169. X. Zhang, T. H. Lee, X. Xiong et al., “Methamphetamine induces long-term changes in GABAA receptor α2 subunit and GAD67 expression,” Biochemical and Biophysical Research Communications, vol. 351, no. 1, pp. 300–305, 2006. View at Publisher · View at Google Scholar · View at Scopus
  170. S. Heysieattalab, N. Naghdi, M.-R. Zarrindast, A. Haghparast, S. E. Mehr, and H. Khoshbouei, “The effects of GABAA and NMDA receptors in the shell-accumbens on spatial memory of METH-treated rats,” Pharmacology Biochemistry and Behavior, vol. 142, pp. 23–35, 2016. View at Publisher · View at Google Scholar · View at Scopus
  171. D. A. Finn and J. C. Crabbe, “Exploring alcohol withdrawal syndrome,” Alcohol Health & Research World, vol. 21, no. 2, pp. 149–156, 1997. View at Google Scholar · View at Scopus
  172. M. A. Kashem, S. Ahmed, N. Sultana et al., “Metabolomics of neurotransmitters and related metabolites in post-mortem tissue from the dorsal and ventral striatum of alcoholic human brain,” Neurochemical Research, vol. 41, no. 1-2, pp. 385–397, 2016. View at Publisher · View at Google Scholar · View at Scopus
  173. J. Liang, A. Kerstin Lindemeyer, A. Suryanarayanan et al., “Plasticity of GABAA receptor-mediated neurotransmission in the nucleus accumbens of alcohol-dependent rats,” Journal of Neurophysiology, vol. 112, no. 1, pp. 39–50, 2014. View at Publisher · View at Google Scholar · View at Scopus
  174. J. Liang, V. N. Marty, Y. Mulpuri, R. W. Olsen, and I. Spigelman, “Selective modulation of GABAergic tonic current by dopamine in the nucleus accumbens of alcohol-dependent rats,” Journal of Neurophysiology, vol. 112, no. 1, pp. 51–60, 2014. View at Publisher · View at Google Scholar · View at Scopus
  175. L. Adermark, S. Jonsson, B. Söderpalm, and M. Ericson, “Region-specific depression of striatal activity in Wistar rat by modest ethanol consumption over a ten-month period,” Alcohol, vol. 47, no. 4, pp. 289–298, 2013. View at Publisher · View at Google Scholar · View at Scopus
  176. J. A. Wasielewski and F. A. Holloway, “Alcohol's interactions with circadian rhythms—a focus on body temperature,” Alcohol Research and Health, vol. 25, no. 2, pp. 94–100, 2001. View at Google Scholar · View at Scopus
  177. A. M. Rosenwasser, “Alcohol, antidepressants, and circadian rhythms. Human and animal models,” Alcohol Research & Health, vol. 25, no. 2, pp. 126–135, 2001. View at Google Scholar · View at Scopus
  178. E. M. Jones, D. Knutson, and D. Haines, “Common problems in patients recovering from chemical dependency,” American Family Physician, vol. 68, no. 10, pp. 1971–1978, 2003. View at Google Scholar · View at Scopus
  179. T. J. Baird and D. V. Gauvin, “Characterization of cocaine self-administration and pharmacokinetics as a function of time of day in the rat,” Pharmacology Biochemistry and Behavior, vol. 65, no. 2, pp. 289–299, 2000. View at Publisher · View at Google Scholar · View at Scopus
  180. J. J. Gamsby, E. L. Templeton, L. A. Bonvini et al., “The circadian Per1 and Per2 genes influence alcohol intake, reinforcement, and blood alcohol levels,” Behavioural Brain Research, vol. 249, pp. 15–21, 2013. View at Publisher · View at Google Scholar · View at Scopus
  181. G. Colombo, P. Maccioni, C. Acciaro et al., “Binge drinking in alcohol-preferring sP rats at the end of the nocturnal period,” Alcohol, vol. 48, no. 3, pp. 301–311, 2014. View at Publisher · View at Google Scholar · View at Scopus
  182. W. J. Lynch, M. J. Girgenti, F. J. Breslin, S. S. Newton, and J. R. Taylor, “Gene profiling the response to repeated cocaine self-administration in dorsal striatum: a focus on circadian genes,” Brain Research, vol. 1213, pp. 166–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  183. V. Yuferov, T. Kroslak, K. Steven Laforge, Y. Zhou, A. Ho, and M. J. Kreek, “Differential gene expression in the rat caudate putamen after 'binge' cocaine administration: advantage of triplicate microarray analysis,” Synapse, vol. 48, no. 4, pp. 157–169, 2003. View at Publisher · View at Google Scholar · View at Scopus
  184. R. W. Logan, N. Edgar, A. G. Gillman, D. Hoffman, X. Zhu, and C. A. McClung, “Chronic stress induces brain region-specific alterations of molecular rhythms that correlate with depression-like behavior in mice,” Biological Psychiatry, vol. 78, no. 4, pp. 249–258, 2015. View at Publisher · View at Google Scholar · View at Scopus
  185. A. Schnell, F. Sandrelli, V. Ranc et al., “Mice lacking circadian clock components display different mood-related behaviors and do not respond uniformly to chronic lithium treatment,” Chronobiology International, vol. 32, no. 8, pp. 1075–1089, 2015. View at Publisher · View at Google Scholar · View at Scopus
  186. K. Roybal, D. Theobold, A. Graham et al., “Mania-like behavior induced by disruption of CLOCK,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 15, pp. 6406–6411, 2007. View at Publisher · View at Google Scholar · View at Scopus